Proinflammatory cytokine regulation of cyclic AMP-phosphodiesterase 4 signaling in microglia in vitro and following CNS injury

GLIA

Volumn 60, Issue 12, 2012, Pages 1839-1859

  Ghosh, Mousumi ^a   Garcia Castillo, Daniela ^a   Aguirre, Vladimir ^a   Golshani, Roozbeh ^a   Atkins, Coleen M ^a   Bramlett, Helen M ^a,b   Dietrich, W Dalton ^a   Pearse, Damien D ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

CNS; Cyclic AMP; IL 1 ; Inflammation; Phosphodiesterase; Rolipram; TNF

Indexed keywords

CYTOKINE; INTERLEUKIN 1BETA; PHOSPHODIESTERASE IV; ROLIPRAM; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELLULAR DISTRIBUTION; ENZYME ACTIVITY; IMMUNOBLOTTING; IMMUNOPHENOTYPING; IN VITRO STUDY; INTRACELLULAR SIGNALING; MACROPHAGE; MALE; MICROGLIA; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; TRAUMATIC BRAIN INJURY; UPREGULATION;

ANIMALS; CELL LINE; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM DISEASES; CYCLIC AMP; CYCLIC NUCLEOTIDE PHOSPHODIESTERASES, TYPE 4; CYTOKINES; INFLAMMATION MEDIATORS; MALE; MICE; MICROGLIA; RATS; RATS, INBRED F344; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SPINAL CORD INJURIES;

EID: 84867637397     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22401     Document Type: Article

References (74)

1. Aloisi F. 2001. Immune function of microglia. Glia 36: 165-179.
2. Aronoff DM, Canetti C, Peters-Golden M. 2004. Prostaglandin E2 inhibits alveolar macrophage phagocytosis through an E-prostanoid 2 receptor-mediated increase in intracellular cyclic AMP. J Immunol 173: 559-565.
3. Arp J, Kirchhof MG, Baroja ML, Nazarian SH, Chau TA, Strathdee CA, Ball EH, Madrenas J. 2003. Regulation of T-cell activation by phosphodiesterase 4B2 requires its dynamic redistribution during immunological synapse formation. Mol Cell Biol 23: 8042-8057.
4. Atkins CM, Oliva AA Jr, Alonso OF, Pearse DD, Bramlett HM, Dietrich WD. 2007. Modulation of the cAMP signaling pathway after traumatic brain injury. Exp Neurol 208: 145-158.
5. Baillie GS, MacKenzie SJ, McPhee I, Houslay MD. 2000. Sub-family selective actions in the ability of Erk2 MAP kinase to phosphorylate and regulate the activity of PDE4 cyclic AMP-specific phosphodiesterases. Br J Pharmacol 131: 811-819.
6. Bao F, Fleming JC, Golshani R, Pearse DD, Kasabov L, Brown A, Weaver LC. 2011. A selective phosphodiesterase-4 inhibitor reduces leukocyte infiltration, oxidative processes, and tissue damage after spinal cord injury. J Neurotrauma 28: 1035-1049.
7. Barakat DJ, Gaglani SM, Neravetla SR, Sanchez AR, Andrade CM, Pressman Y, Puzis R, Garg MS, Bunge MB, Pearse DD. 2005. Survival, integration, and axon growth support of glia transplanted into the chronically contused spinal cord. Cell Transplant 14: 225-240.
8. Bartholdi D, Schwab ME. 1997. Expression of pro-inflammatory cytokine and chemokine mRNA upon experimental spinal cord injury in mouse: An in situ hybridization study. Eur J Neurosci 9: 1422-1438.
9. Baud V, Karin M. 2001. Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol 11: 372-377.
10. Bethea JR, Nagashima H, Acosta MC, Briceno C, Gomez F, Marcillo AE, Loor K, Green J, Dietrich WD. 1999. Systemically administered interleukin-10 reduces tumor necrosis factor-alpha production and significantly improves functional recovery following traumatic spinal cord injury in rats. J Neurotrauma 16: 851-863.
11. Bourne HR, Lichtenstein LM, Melmon KL, Henney CS, Weinstein Y, Shearer GM. 1974. Modulation of inflammation and immunity by cyclic AMP. Science 5: 19-28.
12. Breder CD, Tsujimoto M, Terano Y, Scott DW, Saper CB. 1993. Distribution and characterization of tumor necrosis factor-alpha-like immunoreactivity in the murine central nervous system. J Comp Neurol 337: 543-567.
13. Caggiano AO, Kraig RP. 1999. Prostaglandin E receptor subtypes in cultured rat microglia and their role in reducing lipopolysaccharide-induced interleukin-1beta production. J Neurochem 72: 565-575.
14. Chandrasekaran A, Toh KY, Low SH, Tay SK, Brenner S, Goh DL. 2008. Identification and characterization of novel mouse PDE4D isoforms: Molecular cloning, subcellular distribution and detection of isoform-specific intracellular localization signals. Cell Signal 20: 139-153.
15. Damoiseaux JG, Döpp EA, Calame W, Chao D, MacPherson GG, Dijkstra CD. 1994. Rat macrophage lysosomal membrane antigen recognized by monoclonal antibody ED1. Immunology 83: 140-147.
16. Dopp JM, Mackenzie-Graham A, Otero GC, Merrill JE. 1997. Differential expression, cytokine modulation, and specific functions of type-1 and type-2 tumor necrosis factor receptors in rat glia, J. Neuroimmunol 75: 104-112.
17. D'Sa C, Tolbert LM, Conti M, Duman RS. 2002. Regulation of cAMP-specific phosphodiesterases type 4B and 4D (PDE4) splice variants by cAMP signaling in primary cortical neurons. J Neurochem 81: 745-757.
18. Dunne A, O'Neill LA. 2003. The interleukin-1 receptor/Toll-like receptor superfamily: Signal transduction during inflammation and host defense. Sci STKE 25: 171.
19. Ghosh M, Tuesta LM, Puentes R, Patel S, Melendez K, El Maarouf A, Rutishauser U, Pearse DD. 2012. Extensive cell migration, axon regeneration, and improved function with polysialic acid-modified Schwann cells after spinal cord injury. Glia 60: 979-992.
20. Ghosh P, Pearse DD. 2010. Cyclic AMP-specific PDEs: A promising therapeutic target for CNS repair. Transl Neurosci 1: 101-105.
21. Goodman JC, Van M, Gopinath SP, Robertson CS. 2008. Pro-inflammatory and pro-apoptotic elements of the neuroinflammatory response are activated in traumatic brain injury. Acta Neurochir Suppl 102: 437-439.
22. Gruner JA. 1992. A monitored contusion model of spinal cord injury in the rat. J Neurotrauma 9: 123-126.
23. Hannibal J, Jessop DS, Fahrenkrug J, Harbuz MS, Larsen PJ. 1999. PACAP gene expression in neurons of the rat hypothalamo-pituitary-adrenocortical axis is induced by endotoxin and interleukin-1beta. Neuroendocrinology 70: 73-82.
24. Hurley SD, Walter SA, Semple-Rowland SL, Streit WJ. 1999. Cytokine transcripts expressed by microglia in vitro are not expressed by ameboid microglia of the developing rat central nervous system. Glia 25: 304-309.
25. Huston E, Lynch MJ, Mohamed A, Collins DM, Hill EV, MacLeod R, Krause E, Baillie GS, Houslay MD. 2008. EPAC and PKA allow cAMP dual control over DNA-PK nuclear translocation. Proc Natl Acad Sci USA 105: 12791-12796.
26. Jin SL, Conti M. 2002. Induction of the cyclic nucleotide phosphodiesterase PDE4B is essential for LPS-activated TNF-alpha responses. Proc Natl Acad Sci USA 28: 7628-7633.
27. Jin SL, Lan L, Zoudilova M, Conti M. 2005. Specific role of phosphodiesterase 4B in lipopolysaccharide-induced signaling in mouse macrophages. J Immunol 175: 1523-1531.
28. Jones LL, Banati RB, Graeber MB, Bonfanti L, Raivich G, Kreutzberg GW. 1997. Population control of microglia: Does apoptosis play a role? J Neurocytol 26: 755-770.
29. Kinoshita K, Chatzipanteli K, Vitarbo E, Truettner JS, Alonso OF, Dietrich WD. 2002. Interleukin-1beta messenger ribonucleic acid and protein levels after fluid-percussion brain injury in rats: Importance of injury severity and brain temperature. Neurosurgery 51: 195-203.
30. Kita T, Liu L, Tanaka N, Kinoshita Y. 1997. The expression of tumor necrosis factor-alpha in the rat brain after fluid percussive injury. Int J Legal Med 110: 305-311.
31. Kleppisch T. 2009. Phosphodiesterases in the central nervous system. Handb Exp Pharmacol 191: 71-92.
32. Kreutzberg GW. Microglia: 1996. A sensor for pathological events in the CNS. Trends Neurosci 19: 312-318.
33. Le Jeune IR, Shepherd M, Van Heeke G, Houslay MD, Hall IP. 2002. Cyclic AMP-dependent transcriptional up-regulation of phosphodiesterase 4D5 in human airway smooth muscle cells. Identification and characterization of a novel PDE4D5 promoter. J Biol Chem 277: 35980-35989.
34. Levi G, Minghetti L, Aloisi F. 1998. Regulation of prostanoid synthesis in microglial cells and effects of prostaglandin E2 on microglial functions. Biochimie 80: 899-904.
35. Londesborough J, Jönkkäri L. 1982. Low Km cyclic AMP phosphodiesterase of yeast may be bound to ribosomes associated with the nucleus. Mol Cell Biochem 23: 65-71.
36. Lucin KM, Wyss-Coray T. 2009. Immune activation in brain aging and neurodegeneration: Too much or too little? Neuron 64: 110-122.
37. Lugnier C, Keravis T, Le Bec A, Pauvert O, Proteau S, Rousseau E. 1999. Characterization of cyclic nucleotide phosphodiesterase isoforms associated to isolated cardiac nuclei. Biochim Biophys Acta 16: 431-446.
38. Lupidi G, Eufemi M, Luciani S, Ferraro A, Riva F. 1990. 3′-5′ cAMP phosphodiesterase in pig liver nuclei. Ital J Biochem 39: 30-37.
39. Ma D, Wu P, Egan RW, Billah MM, Wang P. 1999. Phosphodiesterase 4B gene transcription is activated by lipopolysaccharide and inhibited by interleukin-10 in human monocytes. Mol Pharmacol 55: 50-57.
40. MacKenzie SJ, Houslay MD. 2000. Action of rolipram on specific PDE4 cAMP phosphodiesterase isoforms and on the phosphorylation of cAMP-response-element-binding protein (CREB) and p38 mitogen-activated protein (MAP) kinase in U937 monocytic cells. Biochem J 347: 571-578.
41. McCahill A, Campbell L, McSorley T, Sood A, Lynch MJ, Li X, Yan C, Baillie GS, Houslay MD. 2008. In cardiac myocytes, cAMP elevation triggers the down-regulation of transcripts and promoter activity for cyclic AMP phosphodiesterase-4A10 (PDE4A10). Cell Signal 11: 2071-2083.
42. Mecha M, Iñigo PM, Mestre L, Hernangómez M, Borrell J, Guaza C. 2011. An easy and fast way to obtain a high number of glial cells from rat cerebral tissue: A beginners approach. doi: 10.1038/protex.2011.218.
43. Minguet S, Huber M, Rosenkranz L, Schamel WW, Reth M, Brummer T. 2005. Adenosine and cAMP are potent inhibitors of the NF-kappa B pathway downstream of immunoreceptors. Eur J Immunol 35: 31-41.
44. Neumann M, Grieshammer T, Chuvpilo S, Kneitz B, Lohoff M, Schimpl A, Franza BRJr, Serfling E. 1995. RelA/p65 is a molecular target for the immunosuppressive action of protein kinase A. EMBO J 14: 1991-2004.
45. Ortis F, Naamane N, Flamez D, Ladrière L, Moore F, Cunha DA, Colli ML, Thykjaer T, Thorsen K, Orntoft TF, Eizirik DL. 2010. Cytokines interleukin-1beta and tumor necrosis factor-alpha regulate different transcriptional and alternative splicing networks in primary beta-cells. Diabetes 59: 358-374.
46. Pang XP, Ross NS, Park M, Juillard GJ, Stanley TM, Hershman JM. 1992. Tumor necrosis factor-alpha activates nuclear factor kappa B and induces manganous superoxide dismutase and phosphodiesterase mRNA in human papillary thyroid carcinoma cells. J Biol Chem 267: 12826-12830.
47. Patel V, Joseph G, Patel A, Patel S, Bustin D, Mawson D, Tuesta LM, Puentes R, Ghosh M, Pearse DD. 2010. Suspension matrices for improved Schwann-cell survival after implantation into the injured rat spinal cord. J Neurotrauma 27: 789-801.
48. Patrizio M, Costa T, Levi G. 1995. Interferon-gamma and lipopolysaccharide reduce cAMP responses in cultured glial cells: Reversal by a type IV phosphodiesterase inhibitor. Glia 14: 94-100.
49. Patrizio M. 2004. Tumor necrosis factor reduces cAMP production in rat microglia. Glia 48: 241-249.
50. Pearse DD, Bushell G, Leah JD. 2001. Jun, Fos and Krox in the thalamus after C-fiber stimulation: Coincident-input-dependent expression, expression across somatotopic boundaries, and nucleolar translocation. Neuroscience 107: 143-159.
51. Pearse DD, Pereira FC, Stolyarova A, Barakat DJ, Bunge MB. 2004a. Inhibition of tumour necrosis factor-alpha by antisense targeting produces immunophenotypical and morphological changes in injury-activated microglia and macrophages. Eur J Neurosci 20: 3387-3396.
52. Pearse DD, Pereira FC, Marcillo AE, Bates ML, Berrocal YA, Filbin MT, Bunge MB. 2004b. cAMP and Schwann cells promote axonal growth and functional recovery after spinal cord injury. Nat Med 10: 610-616.
53. Pearse D, Jarnagin K. 2010. Abating progressive tissue injury and preserving function after CNS trauma: The role of inflammation modulatory therapies. Curr Opin Investig Drugs 11: 1207-1210.
54. Pineau I, Lacroix S. 2007. Proinflammatory cytokine synthesis in the injured mouse spinal cord: Multiphasic expression pattern and identification of the cell types involved. J Comp Neurol 500: 267-285.
55. Reyes-Irisarri E, Sánchez AJ, García-Merino JA, Mengod G. 2007. Selective induction of cAMP phosphodiesterase PDE4B2 expression in experimental autoimmune encephalomyelitis. J Neuropathol Exp Neurol 66: 923-931.
56. Rice T, Larsen J, Rivest S, Yong VW. 2007. Characterization of the early neuroinflammation after spinal cord injury in mice. J Neuropathol Exp Neurol 66: 184-195.
57. Schaal SM, Kitay BM, Cho KS, Lo TPJr, Barakat DJ, Marcillo AE, Sanchez AR, Andrade CM, Pearse DD. 2007. Schwann cell transplantation improves reticulospinal axon growth and forelimb strength after severe cervical spinal cord contusion. Cell Transplant 16: 207-228.
58. Sebastiani G, Morissette C, Lagacé C, Boulé M, Ouellette MJ, McLaughlin RW, Lacombe D, Gervais F, Tremblay P. 2006. The cAMP-specific phosphodiesterase 4B mediates Abeta-induced microglial activation. Neurobiol Aging 27: 691-701.
59. Selmaj K, Raine CS, Farooq M, Norton WT, Brosnan CF. 1991. Cytokine cytotoxicity against oligodendrocytes. Apoptosis induced by lymphotoxin. J Immunol 147: 1522-1529.
60. Semmler J, Wachtel H, Endres S. 1993 The specific type IV phosphodiesterase inhibitor rolipram suppresses tumor necrosis factor-alpha production by human mononuclear cells. Int J Immunopharmacol 15: 409-413.
61. Serezani CH, Ballinger MN, Aronoff DM, Peters-Golden M. 2008. Cyclic AMP: Master regulator of innate immune cell function. Am J Respir Cell Mol Biol 39: 127-132.
62. Sharif SF, Hariri RJ, Chang VA, Barie PS, Wang RS, Ghajar JB. 1993. Human astrocyte production of tumour necrosis factor-alpha, interleukin-1 beta, and interleukin-6 following exposure to lipopolysaccharide endotoxin. Neurol Res 15: 109-112.
63. Steininger TS, Stutz H, Kerschbaum HH. 2011. Beta-adrenergic stimulation suppresses phagocytosis via Epac activation in murine microglial cells. Brain Res 1407: 1-12.
64. Streit WJ, Semple-Rowland SL, Hurley SD, Miller RC, Popovich PG, Stokes BT. 1998. Cytokine mRNA profiles in contused spinal cord and axotomized facial nucleus suggest a beneficial role for inflammation and gliosis. Exp Neurol 152: 74-87.
65. Vitarbo EA, Chatzipanteli K, Kinoshita K, Truettner JS, Alonso OF, Dietrich WD. 2004. Tumor necrosis factor alpha expression and protein levels after fluid percussion injury in rats: The effect of injury severity and brain temperature. Neurosurgery 55: 416-424.
66. Wajant H, Pfizenmaier K, Scheurich P. 2003. Tumor necrosis factor signaling. Cell Death Differ 10: 45-65.
67. Walker WS, Gatewood J, Olivas E, Askew D, Havenith CEG. 1995. Mouse microglial cell lines differing in constitutive and interferon-γ-inducible antigen-presenting activities for naïve and memory CD4+ and CD8+ T cell. J Neuroimmunol 63: 163-174.
68. Wang C X, Nuttin B, Heremans H, Dom R, Gybels J. 1996. Production of tumor necrosis factor in spinal cord following traumatic injury in rats. J Neuroimmunol 69: 151-156.
69. Wang P, Wu P, Ohleth KM, Egan RW, Billah MM. 1999. Phosphodiesterase 4B2 is the predominant phosphodiesterase species and undergoes differential regulation of gene expression in human monocytes and neutrophils. Mol Pharmacol 56: 170-174.
70. Wang XF, Huang LD, Yu PP, Hu JG, Yin L, Wang L, Xu XM, Lu PH. 2006. Upregulation of type I interleukin-1 receptor after traumatic spinal cord injury in adult rats. Acta Neuropathol 111: 220-228.
71. Weber A, Wasiliew P, Kracht M. 2010. Interleukin-1 (IL-1) pathway. Sci Signal 3: 105-110.
72. Wen AY, Sakamoto KM, Miller LS. 2010. The role of the transcription factor CREB in immune function. J Immunol 185: 6413-6419.
73. Whitaker CM, Beaumont E, Wells MJ, Magnuson DS, Hetman M, Onifer SM. 2008. Rolipram attenuates acute oligodendrocyte death in the adult rat ventrolateral funiculus following contusive cervical spinal cord injury. Neurosci Lett 438: 200-204.
74. Yakovlev AG, Faden AI. 1994. Sequential expression of c-fos proto-oncogene, TNF-alpha, and dynorphin genes in spinal cord following experimental traumatic injury. Mol Chem Neuropathol 23: 179-190.